Kaufman's Atlas of Mouse Development Supplement

With Coronal Sections
Academic Press
  • 1. Auflage
  • |
  • erschienen am 23. September 2015
  • |
  • 344 Seiten
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978-0-12-800913-0 (ISBN)
Kaufman's Atlas of Mouse Development: With Coronal Sections continues the stellar reputation of the original Atlas by providing updated, in-depth anatomical content and morphological views of organ systems.The publication offers written descriptions of the developmental origins of the organ systems alongside high-resolution images for needed visualization of developmental processes. Matt Kaufman himself has annotated the coronal images in the same clear, meticulous style of the original Atlas. Kaufman's Atlas of Mouse Development: With Coronal Sections follows the original Atlas as a continuation of the standard in the field for developmental biologists and researchers across biological and biomedical sciences studying mouse development.
  • Provides high-resolution images for best visualization of key developmental processes and structures
  • Offers in-depth anatomy and morphological views of organ systems
  • Written descriptions convey developmental origins of the organ systems
  • Englisch
  • San Diego
  • |
  • USA
Elsevier Science
  • 79,84 MB
978-0-12-800913-0 (9780128009130)
0128009136 (0128009136)
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  • Front Cover
  • Kaufman's Atlas of Mouse Development Supplement
  • Copyright Page
  • Dedication
  • Contents
  • List of Contributors
  • 1 Introduction
  • 2 Coronal Sections
  • Introduction
  • Methods
  • Results
  • Discussion
  • Acknowledgments
  • References
  • 3 A Revised Staging of Mouse Development Before Organogenesis
  • Introduction
  • Methods
  • Overview of the Revised Staging System, TS1-12
  • Anatomy of Stages with Representative Molecular Markers
  • Preimplantation Stages: TS1-5, E0 to E3.5 (Figure 3.1)
  • From Implantation to the Prestreak Stage: TS6-9a, E4.5-6.5 (Figure 3.2)
  • Early Primitive Streak to Late Pre-Headfold. TS9b-11b, E 6.5-E7.5 (Figure 3.3)
  • Early Headfold to Early Somitogenesis. TS11a-12, E7.5-8 (Figure 3.4)
  • Timing and Litter Variation
  • Discussion
  • Acknowledgments
  • References
  • 4 Development of Early Embryonic Lineages
  • Introduction
  • Preimplantation Development
  • Formation of outer and inner cells of the blastocyst (TS3-4 E2.5-3)
  • Formation of the primitive endoderm (TS4-5 E3-3.5)
  • Postimplantation Development
  • Implantation (TS6 E4.5)
  • Specification of the embryonic anteroposterior axis (by TS7d E5.75)
  • Initiation of gastrulation (TS9a-b E6.25-6.5)
  • Formation of definitive endoderm (TS9b-10b E6.5-7.0)
  • Formation of the primitive central nervous system (TS9a E6.5 onwards)
  • Formation of mesoderm (TS9b E6.5 onward)
  • Amnion formation (TS9b-11a E6.5-7.5)
  • Function of the node (TS9b-TS12 E6.5-8.0)
  • The notochord: Axial mesendoderm (TS10a-TS12 E7.0-8.0)
  • Left/right patterning (TS11d-TS12 E7.5-8.0)
  • Initiation of somitogenesis and the restriction of potency in the epiblast (TS11d E8.0 onwards)
  • Discussion and prospects
  • Acknowledgment
  • References
  • 5 The Alimentary Canal
  • Introduction
  • Current Views and Molecular Mechanisms of Developing Gut Anatomy
  • Morphogenesis and patterning of the gut tube
  • Foregut morphogenesis and patterning
  • Midgut morphogenesis and patterning
  • Hindgut morphogenesis and patterning
  • Additional aspects of alimentary canal patterning
  • Concluding Remarks
  • References
  • 6 The Pancreas
  • Introduction
  • The Current View of the Developmental Anatomy of the Pancreas
  • Formation of the pancreatic anlagen (E8.5-10.5)
  • Morphogenesis and fusion of the pancreatic anlagen (E10.5-17.5)
  • Morphogenesis of the spleen
  • The adult pancreas
  • Discussion
  • References
  • 7 Development of the Heart and Great Vessels
  • Addition of Cardiac Populations to the Early Heart Tube
  • Atrial Septation
  • Formation and Incorporation of the Pulmonary Vein
  • Septation and Separation of the OFT
  • Discussion
  • References
  • 8 Ontogeny of the Hematopoietic System
  • Introduction
  • Sites of Hematopoietic Progenitor Generation
  • The yolk sac: Two waves of hematopoietic progenitors generation
  • The para-aortic splanchnopleura/aorta-gonads-mesonephros: hematopoietic stem cells generation
  • Midgestation Hematopoietic Sites
  • Fetal liver
  • Fetal thymus
  • Late Gestation-Perinatal Hematopoietic Sites
  • Spleen
  • Bone marrow
  • Conclusion
  • Abbreviations
  • References
  • 9 The Reproductive System
  • Introduction
  • The Early Stages
  • Formation of the intermediate mesoderm
  • Primordial germ cells (PGCs)
  • The Indifferent or Bipotential Stage
  • Female Development
  • Male Development
  • Discussion
  • Acknowledgments
  • References
  • 10 Development of the Respiratory System
  • Overview
  • Foregut morphogenesis, and establishment of trachea and primary lung buds
  • Structure of the trachea
  • Branching morphogenesis of the primary lung buds up to about E14.5
  • Branching, morphogenesis, and differentiation of the endoderm after E14.5
  • Development of the pulmonary blood supply, alveologenesis and the early postnatal growth, and remodeling and maturation of ...
  • Lineage tracing of lung mesoderm
  • Differentiation and function of lung mesothelium
  • Discussion
  • References
  • 11 The Urinary System
  • Introduction
  • The Current View of the Developmental Anatomy of the System
  • New Lineage Data
  • Discussion
  • Further Resources
  • References
  • 12 Integument and Associated Integumentary Appendages
  • Introduction: The Structural Diversity of the Mouse Integument
  • Early Integumental Development
  • Specification of discrete domains in the ectoderm
  • Origin, migration, and formation of the dermis
  • Cornea, Interfollicular Skin, and Pilosebaceous Units
  • Cornea
  • Interfollicular skin
  • Different types of hairs, their patterns, and time schedules
  • Molecular mechanisms involved in the formation of hair placodes and subsequent cellular proliferation
  • Hair follicle morphogenesis and segregation of two types of stem cells in the developing pilosebaceous unit
  • Development of the sebaceous gland and related glandular structures
  • The Mammary Gland
  • Formation of the mammary line and associated mesenchyme
  • Formation of the specific types of mammary placodes
  • Formation of the embryonic mammary gland
  • Other Ducted Cutaneous Glands
  • Eccrine sweat glands
  • Salivary glands
  • Lacrimal and Harderian glands
  • Discussion
  • References
  • 13 The Axial Musculoskeletal System
  • Introduction
  • The Current View of the Developmental Anatomy of the System
  • Developmental anatomy of the segmentation process
  • Somite differentiation
  • The sclerotome
  • The dermomyotome and the myotome
  • The syndetome
  • New Lineage Data
  • Sclerotome
  • Dermomyotome and myotome
  • Discussion
  • References
  • 14 Spinal Cord and Peripheral Nervous System
  • Introduction
  • The Current View of the Developmental Anatomy of the Spinal Cord and the Peripheral Nervous System
  • Neurulation and neural tube defects
  • Anteroposterior patterning and segmental organization of the spinal cord
  • Segmental organization of the peripheral nervous system
  • Segmental neural crest cell migration
  • Segmental organization of somatic and sympathetic efferent nerves
  • Development of the parasympathetic nervous system: a special case
  • The enteric nervous system
  • Dorsoventral patterning of the neural tube
  • The development of neuronal pathways within the spinal cord
  • General principles
  • The formation of sensory-motor connections
  • The formation of motor columns
  • Formation of spinal nerves
  • The refinement of connections
  • Discussion
  • Acknowledgments
  • References
  • 15 Limb Development
  • Introduction
  • AnatomicAL Features of the Early Limb Bud
  • Limb Initiation and Specification
  • Limb Outgrowth
  • Proximodistal axis
  • Anteroposterior axis
  • Integrating proximodistal and anteroposterior signaling
  • Dorsoventral axis
  • Programmed cell death
  • Chondrogenesis and joint formation
  • Tendon and ligament development
  • Muscle formation
  • Conclusion
  • References
  • 16 The Craniofacial Region
  • Introduction
  • The Current View of the Developmental Anatomy of the Head and Neck
  • Early morphogenesis of the cranial region and formation of the pituitary and pineal glands
  • Origin of the craniofacial tissue components
  • The embryonic face and pharynx
  • Early development
  • Pharyngeal arches, pouches, and clefts
  • Cranial nerves
  • Melanocytes
  • The skull
  • The skull base
  • The skull vault and face
  • Discussion
  • Acknowledgments
  • References
  • 17 Recent Advances in Palate and Tongue Development
  • Introduction
  • The Current View of the Developmental Anatomy of the Palate and Tongue
  • Palate development
  • Patterning of the palatal shelves
  • Elevation of the palatal shelves
  • Palatal shelf growth: proliferation of the CNCC-derived mesenchyme
  • Palatal fusion
  • Soft palate development
  • Tongue development
  • Myogenic lineage in the developing tongue
  • Cranial neural crest-derived mesenchyme in the developing tongue
  • Myogenic stem cells, tongue disease, and therapeutic perspectives
  • Discussion
  • References
  • 18 The Developmental Anatomy of Teeth
  • Introduction
  • The Current View of the Developmental Anatomy of Teeth
  • The dental lamina
  • Tooth placodes
  • Enamel knots
  • Stem cells in the continuously growing mouse incisor
  • New lineage data
  • Discussion
  • Acknowledgments
  • References
  • 19 Brain Development
  • Introduction
  • The Current View of the Developmental Anatomy of the Mouse Brain
  • Neural Induction, neurulation, and early regionalization
  • The Developmental Anatomy of the Mouse Cerebral Neocortex
  • The origin and migration of cortical neurons
  • Pyramidal cells and radial migration
  • Interneuron generation and tangential migration
  • Cell death during early cortical development
  • Mechanisms Controlling Development of the Mouse Cerebral Neocortex
  • Extrinsic and intrinsic influences on cortical development
  • Thalamic and thalamocortical development
  • Formation of maps in the cortex
  • Connectivity between regions
  • Mouse barrel formation: an example of map formation
  • Plasticity during development
  • Development of the Mouse Cerebellum
  • Cerebellar specification
  • Genesis of the cerebellum
  • The Formation of cerebellar connections
  • Conclusions
  • Acknowledgments
  • References
  • 20 The Visual System
  • Introduction
  • The Current View of the Developmental Anatomy of the Visual System
  • Establishing the Eye Field
  • Signals
  • Transcription Factors
  • Separating the Eye Field
  • Optic Vesicle Patterning and Morphogenesis
  • Optic Cup Development
  • The Lens
  • Lens Placode: Transcription Factors and Signals
  • Lens Placode Invagination
  • Retinal Histogenesis
  • The Optic Nerve and Chiasm
  • RGC Growth to the Optic Nerve
  • The Optic Chiasm
  • Topographic Mapping
  • The Anterior Segment
  • Cornea
  • Iris
  • Signals and Transcription Factors in Anterior Segment Development
  • Accessory Structures
  • Eyelids
  • Extraocular Muscles, Choroid, and Sclera
  • Blood Supply
  • Discussion
  • References
  • 21 Development and Lineage Relationships of the Mouse Inner Ear
  • Introduction
  • Development of the Membranous Labyrinth
  • Cell Fate and Lineage Relationships
  • Contribution from the Neural Crest
  • Future Directions
  • Acknowledgments
  • References
  • 22 Olfactory System Embryonic Development
  • Introduction
  • Current View of the Developmental Anatomy of the Olfactory System
  • A brief scheme of the basic organization of the mature olfactory system
  • Development of the olfactory systems: Neurogenesis
  • Development of the olfactory system: Axon interconnections
  • Discussion
  • Acknowledgments
  • Abbreviations
  • References
  • 23 Textual Anatomics: The Mouse Developmental Anatomy Ontology and the Gene Expression Database for Mouse Development (GXD)
  • Introduction
  • The AnatomicAL Ontology for Mouse Development: Evolution and Current Status
  • Ontology content
  • Hierarchical structure
  • "Abstract" and stage-specific representations
  • Ontology extension and refinement
  • Current status
  • The Gene Expression Database for Mouse Development (GXD)
  • The mouse developmental anatomy browser
  • The Gene Expression Data Query Form
  • Expression search result summaries, assay details, and images
  • Gene expression matrix views
  • Anatomy-Based Data Integration: Other Data Sets and Resources
  • Future Directions
  • Anatomy ontology development
  • GXD and anatomicAL integration with other resources
  • Acknowledgments
  • References
  • 24 Digital Graphical Resources and Developmental Anatomy in the Mouse
  • Introduction
  • 3D Digital Atlas Models and Developmental Anatomy
  • Kaufman eHistology Atlas
  • Use Case: Identifying Developmentally Significant Molecular Anatomy Profiles Using Digital Atlas Resources
  • Emage
  • Gudmap
  • Future Work
  • Visualizing anatomicAL progression through development
  • Community annotation and data sharing of digital atlas resources
  • Acknowledgments
  • References
  • 25 The Informatics of Developmental Phenotypes
  • Introduction
  • What are Developmental Phenotypes?
  • Methods for Capturing Phenotype Information
  • Phenotype Ontologies
  • Challenges in Morphometric Phenotyping
  • Integrating Developmental Phenotypes Within and Across Species
  • Discussion
  • Acknowledgments
  • References
  • Index
  • Back Cover

Coronal Sections

David J. Price1, Elizabeth Graham2, Julie Moss2, Chris Armit2 and Richard Baldock2,    1Centre for Integrative Physiology, The University of Edinburgh, Edinburgh, UK,    2MRC Human Genetics Unit, IGMM, The University of Edinburgh, Edinburgh, UK

The original The Atlas of Mouse Development by Matt Kaufman (MK) included transverse and sagittal sections at multiple stages of development, but only two plates of coronal sections (stages E14.5 (plate 34) and E16.5 (plate 39)). When a revised version of the Atlas was suggested, a survey of users recommended that the series of coronal sections should be extended to include additional stages of development, particularly the brain at E11, E11.5, E12.5, E13.5, and E15.5. This chapter presents these new coronal sections, together with some new sections to extend the E14.5 images provided in the original Atlas. These sections include some original annotations from MK that are supplemented by more detailed brain annotations.


Atlas; ontology; Matt Kaufman; mouse development; histology plates; coronal sections


The Atlas of Mouse Development by Matt Kaufman (MK; Kaufman, 1994) is the defining standard for mouse development and remains an essential text for developmental biologists and biomedical scientists. The Atlas has a series of plates of histological sections through embryos that have been selected to represent each Theiler stage of development. Each image within a plate is carefully annotated with the tissues visible in each section clearly labeled. The original Atlas includes two embryos sectioned coronally at E14.5 and E16.5. When users were asked what should be added to a revised edition of the Atlas, there was a clear demand for additional coronal sections to complete the developmental series in order to make the development of the embryonic brain easier for the research community to understand.

This chapter provides these new coronal sections as a series of plates that can be used in conjunction with the original Atlas and the chapters of this volume. Before ceasing work on the revised Atlas (now presented as this Atlas Supplement), MK selected the embryos, specified the sections that were most illustrative and should be used for these new plates, and provided some preliminary annotation. Here, we have taken that selection and extended the annotation.

The printed version of these sections follows the style of the Atlas with each image labeled with lines and numbers, with each number linked to an annotation on the same two-page view. These coronal sections only show the head-region of the section so that the brain is printed at the highest possible resolution. We also provide the fully annotated, high-resolution images online within a "zoom" style viewer (see www.emouseatlas.org).

While MK's annotations in the original Atlas were given as short descriptions, the plates here use the anatomical terms defined by the Edinburgh Mouse Atlas Project (EMAP) mouse developmental anatomy ontology (see Chapter 23 and Hayamizu et al., 2013). This ontology uses a controlled vocabulary, and this has been extended to include some new annotations shown here. An advantage of using the EMAP ontology descriptions for labeling tissues is that the online visualization of each section is directly linked (through the hidden ontology term IDs) to other database resources, and this allows a user to, for example, directly query gene-expression in any anatomical component. The EMAP ontology also describes the stage range for specific anatomical components, and this allows researchers to follow, in order of appearance, the various anatomical components of the developing mouse embryo. We hope that the use of EMAP ontology terms will allow researchers to explore embryonic development in new ways.


To generate the new coronal sections, we used C57Bl6J×CBA F1 embryos that were collected, fixed, and washed in the same way as those for The Atlas of Mouse Development (Kaufman, 1994). Embryos were dehydrated through an ethanol gradient, cleared in xylene, then infiltrated and embedded in paraffin wax (56°C melting point). They were then embedded on their side on a layer of setting wax in molds of suitable size, and this allowed the embryo to be oriented for coronal sectioning. The trimmed wax block was mounted on a wooden chuck and attached to the microtome (Leica RM2264 motorized with retraction and microscope attachment). Starting at the front of the embryo, serial sections were cut at 7 µm, using the motorized setting, directly onto distilled water (room temperature) in a trough specifically designed to keep section loss to a minimum (this was manufactured "in house" to fit the disposable knife holder).

Strings of sections were removed from the trough on a glass slide and carefully introduced into a floating-out bath at 42-45°C where they were allowed to stretch out for a few seconds. Time and temperature were carefully monitored to make the stretching consistent. The sections were then aligned on a cleaned glass slide, withdrawn from the bath, and dried vertically at room temperature overnight. Before staining, the slides were placed in an oven at 60°C for 2 h, dewaxed in xylene, and rehydrated through an ethanol gradient to water. The sections were stained in Mayer's Haemalum for 5 min, and aqueous Eosin Y for 3 min, then dehydrated, cleared in xylene, and mounted in DPX (coverslip thickness No. 1.5: 0.13-0.17 mm).

Once the mountant had completely set, the slides were digitized using the Olympus DotSlide, which capture a complete image of each section by automated scanning over the area of tissue. To optimize the digital image focus, we manually set focus points for each section then the scanning was performed with either a ×10 or a ×20 objective resulting in image pixel resolutions of 0.32 and 0.16 µm, respectively.

The DotSlide images were output to "tiff format" and converted to multiresolution tiled "pyramidal" format using the VIPS image processing software (Martinez and Cupitt, 2005). This provides the required tiled format for a zoom-viewer interface using the IIP3D server (Husz et al., 2012). In addition, we developed a bespoke MySQL database to hold the plate information and annotations. The interface used to deliver the coronal image can be configured to allow editorial placement of points associated with any ontology term.


The following table lists the stages covered by these additional coronal sections and some additional data for each embryo.

E11.0 (TS18) S1 a,b 6,8 4.0 12 Stage 18 (121-129) E11.5 (TS19) S2 a-c 10,12,14 4.4 11 Stage 19 (131-144) E12.5 (TS20) S3 a-d 16,18,20,22 7.9 19 Stage 20 (145-156) E13.5 (TS22) S4 a-d 24,26,28,30 8.2 16 Stage 21 (157-176) E14.5 (TS23) S5 a-d 32,34,36,38 10.2 16 Stage 22 (177-210) E15.5 (TS25) S6 a-e 40,42,44,46,48 11.8 20 Stage 23 (211-248)


These coronal sections extend the series of coronal sections provided in the original The Atlas of Mouse Development. Low-resolution images are available in the Supplement, while high-resolution versions are available from the eMouseAtlas Web site (www.emouseatlas.org) and these show the annotations identified by the matching number in the plates shown here. The same images available at much higher resolution on the Internet are an open-access community resource available freely for scientific and educational purposes. In this context, we hope to invite expert developmental anatomists to contribute to the resource to enhance the annotations available and so increase our knowledge of developmental anatomy.


We thank Allyson Ross for preparing and sectioning the embryos and Nick Burton for developing the editing viewer that enabled anatomical terms to be selected and annotations to be placed on images.


1. Hayamizu TF, Wicks MN, Davidson DR, Burger A, Ringwald M, Baldock RA. EMAP/EMAPA ontology of mouse developmental anatomy: 2013 update. J Biomed Semantics. 2013;4:15 In: http://dx.doi.org/10.1186/2041-1480-4-15.

2. Husz ZL, Burton N, Hill W, Milaev N, Baldock RA. Web tools for large-scale 3D biological images and atlases. BMC Bioinformatics. 2012;13:122 In: http://dx.doi.org/10.1186/1471-2105-13-122.

3. Kaufman MH. The Atlas of Mouse Development revised ed. London: Academic Press; 1994.

4. Martinez, K., Cupitt, J., 2005. VIPS-a highly tuned image processing software architecture. In: Conference Proceedings, IEEE International Conference on Image Processing 2, Genova, pp....

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